Hostname: page-component-78c5997874-g7gxr Total loading time: 0 Render date: 2024-11-05T09:13:21.022Z Has data issue: false hasContentIssue false

Differential association between circulating testosterone and infection risk by several viruses in natural cat populations: a behavioural-mediated effect?

Published online by Cambridge University Press:  03 January 2013

E. HELLARD*
Affiliation:
Laboratoire de Biométrie et Biologie Evolutive, Université de Lyon, Université Lyon I, CNRS, UMR 5558, 43 Bd du 11 novembre 1918, 69622, Villeurbanne, France
D. FOUCHET
Affiliation:
Laboratoire de Biométrie et Biologie Evolutive, Université de Lyon, Université Lyon I, CNRS, UMR 5558, 43 Bd du 11 novembre 1918, 69622, Villeurbanne, France
B. REY
Affiliation:
Laboratoire de Biométrie et Biologie Evolutive, Université de Lyon, Université Lyon I, CNRS, UMR 5558, 43 Bd du 11 novembre 1918, 69622, Villeurbanne, France
A. MOUCHET
Affiliation:
Laboratoire de Biométrie et Biologie Evolutive, Université de Lyon, Université Lyon I, CNRS, UMR 5558, 43 Bd du 11 novembre 1918, 69622, Villeurbanne, France
H. POULET
Affiliation:
Merial, Laboratoire de Lyon Gerland, 254 rue Marcel Mérieux, 69007 Lyon, France
D. PONTIER
Affiliation:
Laboratoire de Biométrie et Biologie Evolutive, Université de Lyon, Université Lyon I, CNRS, UMR 5558, 43 Bd du 11 novembre 1918, 69622, Villeurbanne, France
*
*Corresponding author: Laboratoire de Biométrie et Biologie Evolutive, Université de Lyon, Université Lyon I, CNRS, UMR 5558, 43 Bd du 11 novembre 1918, 69622, Villeurbanne, France. Tel: +33 (0) 4 72 44 84 37. Fax: +33 (0) 4 72 43 13 88. E-mail: [email protected]

Summary

Testosterone is involved in the development and expression of physiological, morphological and behavioural traits. High levels are often associated with high infection risk and/or intensity, suggesting a trade-off between sexual traits and immunity. Classically invoked mechanisms are immunological or behavioural, i.e., testosterone increases susceptibility or resistance to parasites via an impact on immunity or modulates behaviours involved in parasite transmission. However, studies report contrasted patterns. Given its modes of action and the diversity of host-parasite interactions, testosterone should not act similarly on all interactions. To reduce host and context diversity, we studied 3 viruses in the same cat population: the aggressively transmitted Feline Immunodeficiency virus (FIV), and the Feline Calicivirus (FCV) and Herpesvirus (FHV) both transmitted during friendly contacts. Testosterone had a strong effect on the probability of being positive to FIV whereas its effect was significantly weaker on FCV and FHV. These findings demonstrate that testosterone can be differentially associated with parasites of the same type (viruses). The difference we observed was consistent with a behavioural-mediated effect (increased aggressiveness), supporting the idea that the testosterone effect on infection risk is at least partially driven by behavioural mechanisms in our system. Further investigations (e.g., individual immunity measures) are required to confirm this hypothesis.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2013

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Anderson, D. R., Burnham, K. P. and White, G. C. (1994). AIC model selection in overdispersed capture-recapture data. Ecology 75, 17801793. doi: 10.2307/1939637.CrossRefGoogle Scholar
Apanius, V. (1998). Stress and immune defense. Advances in the Study of Behavior 27, 133153.CrossRefGoogle Scholar
Bahi-Jaber, N., Fouchet, D. and Pontier, D. (2008). Stochastic extinction and the selection of the transmission mode in microparasites. Journal of the Royal Society Interface 5, 10311039. doi: 10.1098/rsif.2007.1326.CrossRefGoogle ScholarPubMed
Barber, I. and Dingemanse, N. J. (2010). Parasitism and the evolutionary ecology of animal personality. Philosophical Transactions of the Royal Society, B 365, 40774088. doi: 10.1098/rstb.2010.0182.CrossRefGoogle ScholarPubMed
Bendinelli, M., Pistello, M., Lombardi, S., Poli, A., Garzelli, C., Matteucci, D., Ceccherininelli, L., Malvaldi, G. and Tozzini, F. (1995). Feline immunodeficiency virus – an interesting model for Aids studies and an important cat pathogen. Clinical Microbiology Reviews 8, 87112.CrossRefGoogle Scholar
Brockman, D. K., Whitten, P. L., Richard, A. F. and Schneider, A. (1998). Reproduction in free-ranging male Propithecus verreauxi: the hormonal correlates of mating and aggression. American Journal of Physical Anthropology 105, 137151. doi: 10.1002/(SICI)1096-8644(199802)105:2 < 137::AID-AJPA3 > 3·0.CO;2-S.3.0.CO;2-S>CrossRefGoogle ScholarPubMed
Brown, S. L. and Bradshaw, J. W. S. (1996). Social behaviour in a small colony of neutered feral cats. Journal of the Feline Advisory Bureau 34, 3537.Google Scholar
Buck, C. L. and Barnes, B. M. (2003). Androgen in free-living arctic ground squirrels: seasonal changes and influence of staged male–male aggressive encounters. Hormones and Behavior 43, 318326. doi: 10.1016/S0018-506X(02)00050-8.CrossRefGoogle ScholarPubMed
Buttemer, W. and Astheimer, L. (2000). Testosterone does not affect basal metabolic rate or blood parasite load in captive male white-plumed honeyeaters Lichenostomus penicillatus. Journal of Avian Biology 31, 479488. doi: 10.1034/j.1600-048X.2000.310407.x.CrossRefGoogle Scholar
Casto, J. M., Nolan, V. and Ketterson, E. D. (2001). Steroid hormones and immune function: Experimental studies in wild and captive dark-eyed juncos (Junco hyemalis). American Naturalist 157, 408420. doi: 10.1086/319318.CrossRefGoogle ScholarPubMed
Cavigelli, S. A. and Pereira, M. E. (2000). Mating season aggression and fecal testosterone levels in male ring-tailed lemurs (Lemur catta). Hormones and Behavior 37, 246255. doi: 10.1006/hbeh.2000.1585.CrossRefGoogle ScholarPubMed
Corbett, L. K. (1979). Feeding ecology and social organization of wild cats (Felis silvestris) and domestic cats (Felis catus) in Scotland. Ph.D. thesis. University of Aberdeen, Aberdeen, UK.Google Scholar
Courchamp, F., Artois, M., Yoccoz, N. and Pontier, D. (1998). At-risk individuals in Feline Immunodeficiency Virus epidemiology: Evidence from a multivariate approach in a natural population of domestic cats (Felis catus). Epidemiology and Infection 121, 227236. doi: 10.1017/S0950268898008875.CrossRefGoogle Scholar
Courchamp, F. and Pontier, D. (1994). Feline immunodeficiency virus: an epidemiologic review. Comptes Rendus de L'Académie des Sciences Série Iii-Sciences de la Vie 317, 11231134.Google Scholar
Courchamp, F., Say, L. and Pontier, D. (2000). Transmission of the feline immunodeficiency in a population of cats (Felis catus). Wildlife Research 27, 603611. doi: 10.1071/WR99049.CrossRefGoogle Scholar
Cox, R. and John-Alder, H. (2007). Increased mite parasitism as a cost of testosterone in male striped plateau lizards Sceloporus virgatus. Functional Ecology 21, 327334. doi: 10.1111/j.1365-2435.2007.01251.x.CrossRefGoogle Scholar
Davies, N. B. (1991). Mating system. In Behavioural Ecology, 3rd Edn (ed. Krebs, J. R. and Davies, N. B.), pp. 263294. Blackwell, Oxford, UK.Google Scholar
Easterbrook, J. D., Kaplan, J. B., Glass, G. E., Pletnikov, M. V. and Klein, S. L. (2007). Elevated testosterone and reduced 5-HIAA concentrations are associated with wounding and hantavirus infection in male Norway rats. Hormones and Behavior 52, 474481. doi: 10.1016/j.yhbeh.2007.07.001.CrossRefGoogle ScholarPubMed
Edler, R., Goymann, W., Schwabl, I. and Friedl, T. W. P. (2011). Experimentally elevated testosterone levels enhance courtship behaviour and territoriality but depress acquired immune response in Red Bishops Euplectes orix. Ibis 153, 4658. doi: 10.1111/j.1474-919X.2010.01075.x.CrossRefGoogle Scholar
Flegr, J., Lindová, J. and Kodym, P. (2008). Sex-dependent toxoplasmosis-associated differences in testosterone concentration in humans. Parasitology 135, 427431. doi: 10.1017/S0031182007004064.CrossRefGoogle ScholarPubMed
Fouchet, D., Leblanc, G., Sauvage, F., Guiserix, M., Poulet, H. and Pontier, D. (2010). Using dynamic stochastic modelling to estimate population risk factors in infectious disease: the example of FIV in 15 cat populations. PLoS One 4, 113. doi: 10.1371/journal.pone.0007377.Google Scholar
Fouchet, D., Verrier, D., Ngoubangoye, B., Souquière, S., Makuwa, M., Kazanji, M., Gonzalez, J. and Pontier, D. (2012). Natural simian immunodeficiency virus transmission in mandrills: a family affair? Proceedings of the Royal Society of London, B 279, 34263435. doi: 10.1098/rspb.2012.0963.Google ScholarPubMed
Frank, L., Davidson, J. and Smith, E. (1985). Androgen levels in the spotted hyaena Crocuta crocuta: the influence of social factors. Journal of Zoology 206, 525531. doi: 10.1111/j.1469-7998.1985.tb03556.x.CrossRefGoogle Scholar
Friedman, S. B., Glasgow, L. A. and Grota, L. J. (1972). Differential Susceptibility of Male and Female Mice To Encephalomyocarditis Virus – Effects of Castration, Adrenalectomy, and Administration of Sex-hormones. Infection and Immunity 5, 637644.CrossRefGoogle ScholarPubMed
Fuxjager, M. J., Foufopoulos, J., Diaz-Uriarte, R. and Marler, C. A. (2011). Functionally opposing effects of testosterone on two different types of parasite: implications for the immunocompetence handicap hypothesis. Functional Ecology 25, 132138. doi: 10.1111/j.1365-2435.2010.01784.x.CrossRefGoogle Scholar
Gaskell, R. M. and Povey, R. C. (1977). Experimental induction of feline viral rhinotracheitis virus re-excretion in Fvr-recovered cats. Veterinary Record 100, 128133. doi: 10.1136/vr.100.7.128.CrossRefGoogle ScholarPubMed
Gaskell, R. M. and Povey, R. C. (1982). Transmission of feline viral rhinotracheitis. Veterinary Record 111, 359362. doi: 10.1136/vr.111.16.359.CrossRefGoogle ScholarPubMed
Glass, G. E., Childs, J. E., Korch, G. W. and LeDuc, J. W. (1988). Association of intraspecific wounding with hantaviral infection in wild rats (Rattus norvegicus). Epidemiology and Infection 101, 459–72. doi: 10.1017/S0950268800054418.CrossRefGoogle ScholarPubMed
Grossman, C. J. (1985). Interactions between the gonadal-steroids and the immune system. Science 227, 257261. doi: 10.1126/science.3871252.CrossRefGoogle ScholarPubMed
Hart, B. L. and Barrett, R. E. (1973). Effects of castration on fighting, roaming, and urine spraying in adult male cats. Journal of the American Veterinary Medicine Association 163, 290292.Google ScholarPubMed
Hawley, D., Etienne, R., Ezenwa, V. and Jolles, A. (2011). Does animal behavior underlie covariation between hosts’ exposure to infectious agents and susceptibility to infection? implications for disease dynamics. Integrative and Comparative Biology 51, 528539. doi: 10.1093/icb/icr062.CrossRefGoogle ScholarPubMed
Hellard, E., Fouchet, D., Santin-Janin, H., Tarin, B., Badol, V., Coupier, C., Leblanc, G., Poulet, H. and Pontier, D. (2011). When cats' ways of life interact with their viruses: A study in 15 natural populations of owned and unowned cats (Felis silvestris catus). Preventive Veterinary Medicine 101, 250264. doi: 10.1016/j.prevetmed.2011.04.020.CrossRefGoogle ScholarPubMed
Hirota, Y., Suzuki, T., Chazono, Y. and Bito, Y. (1976). Humoral immune-responses characteristic of testosterone-propionate-treated chickens. Immunology 30, 341348.Google ScholarPubMed
Hughes, V. L. and Randolph, S. E. (2001). Testosterone increases the transmission potential of tick-borne parasites. Parasitology 123, 365371. doi: 10.1017/ S0031182001008599.CrossRefGoogle ScholarPubMed
Kamis, A. B., Ahmad, R. A. and Badrul-Munir, M. Z. (1992). Worm burden and leukocyte response in Angiostrongylus malaysiensis-infected rats: the influence of testosterone. Parasitology Research 78, 388391. doi: 10.1007/BF00931693.CrossRefGoogle ScholarPubMed
Kankova, S., Kodem, P. and Flegr, J. (2011). Direct evidence of Toxoplasma-induced changes in serum testosterone in mice. Experimental Parasitology 128, 181183. doi: 10.1016/j.exppara.2011.03.014.CrossRefGoogle ScholarPubMed
Klein, S. L. (2000). The effects of hormones on sex differences in infection: from genes to behavior. Neuroscience Biobehavioral Reviews 24, 627638. doi: 10.1016/S0149-7634(00)00027-0.CrossRefGoogle Scholar
Klein, S. L. (2004). Hormonal and immunological mechanisms mediating sex differences in parasite infection. Parasite Immunology 26, 247264. doi: 10.1111/j.0141-9838.2004.00710.x.CrossRefGoogle ScholarPubMed
Klein, S. L., Bird, B. H. and Glass, G. E. (2000). Sex differences in Seoul virus infection are not related to adult sex steroid concentrations in Norway rats. Journal of Virology 74, 82138217. doi: 10.1128/JVI.74.17.8213–8217.2000.CrossRefGoogle Scholar
Klukowski, M. and Nelson, C. E. (1998). The challenge hypothesis and seasonal changes in aggression and steroids in male northern fence lizards (Sceloporus undulatus hyacinthinus). Hormones and Behavior 33, 197204. doi: 10.1006/hbeh.1998.1449.CrossRefGoogle ScholarPubMed
Knowles, J. O., McArdle, F., Dawson, S., Carter, S. D., Gaskell, C. J. and Gaskell, R. M. (1991). Studies On the Role of Feline Calicivirus In Chronic Stomatitis In Cats. Veterinary Microbiology 27, 205219. doi: 10.1016/0378-1135(91)90148-9.CrossRefGoogle ScholarPubMed
Lee, K. A. (2006). Linking immune defenses and life history at the levels of the individual and the species. Integrative and Comparative Biology 46, 10001015. doi: 10.1093/icb/icl049.CrossRefGoogle ScholarPubMed
Liberg, O. (1980). Spacing pattern in a population of rural free roaming domestic cats. Oikos 35, 336349. doi: 10.2307/3544649.CrossRefGoogle Scholar
Liberg, O. (1981). Predation and social behaviour in a population of domestic cats. An evolutionary perspective. Ph.D. thesis, University of Lund, Lund, Sweden.Google Scholar
Liberg, O. (1983). Courtship behaviour and sexual selection in the domestic cat. Applied Animal Ethology 10, 117132. doi: 10.1016/0304-3762(83)90116-5.CrossRefGoogle Scholar
Liberg, O., Sandell, M., Pontier, D. and Natoli, E. (2000). Density, spatial organisation and reproductive tactics in the domestic cat and other felids. In The Domestic Cat: the Biology of its Behavior (ed. Turner, D. C. and Bateson, P.), pp. 119147. Cambridge University Press, Cambridge, UK.Google Scholar
Lindstrom, K. M., Krakower, D., Lundstrom, J. O. and Silverin, B. (2001). The effects of testosterone on a viral infection in greenfinches (Carduelis chloris): an experimental test of the immunocompetence-handicap hypothesis. Proceedings of the Royal Society of London, B 268, 207211. doi: 10.1098/rspb.2000.1352.CrossRefGoogle ScholarPubMed
Marler, C. A. and Moore, M. C. (1988). Evolutionary costs of aggression revealed by testosterone manipulations in free-living male lizards. Behavioral Ecology Sociobiology 23, 2126. doi: 10.1007/BF00303053.CrossRefGoogle Scholar
Mehlman, P. T., Higley, J. D., Fernald, B. J., Sallee, F. R., Suomi, S. J. and Linnoila, M. (1997). CSF 5-HIAA, testosterone and sociosexual behaviors in free-ranging male rhesus macaques in the mating season. Psychiatry Research 72, 89102. doi: 10.1016/S0165-1781(97)00084-X.CrossRefGoogle ScholarPubMed
Mougeot, F., Redpath, S. M., Piertney, S. B. and Hudson, P. J. (2005). Separating behavioral and physiological mechanisms in testosterone-mediated trade-offs. American Naturalist 166, 158168. doi: 10.1086/431256.CrossRefGoogle ScholarPubMed
Nakazawa, M., Fantappie, M. R., Freeman, G. L. Jr, Eloi-Santos, S., Olsen, N. J., Kovacs, W. J., Secor, W. E. and Colley, D. G. (1997). Schistosoma mansoni: susceptibility differences between male and female mice can be mediated by testosterone during early infection. Experimental Parasitology 85, 233240. doi: 10.1006/expr.1997.4148.CrossRefGoogle ScholarPubMed
Natoli, E., Say, L., Cafazzo, S., Bonanni, R., Schmid, M. and Pontier, D. (2005). Bold attitude makes male urban feral domestic cats more vulnerable to Feline Immunodeficiency Virus. Neuroscience and Biobehavioral Reviews 29, 151157. doi: 10.1016/j.neubiorev.2004.06.011.CrossRefGoogle ScholarPubMed
Negro, S. S., Caudron, A. K., Dubois, M., Delahaut, P. and Gemmell, N. J. (2010). Correlation between male social status, testosterone levels, and parasitism in a dimorphic polygynous mammal. Plos One 5, e12507. doi: 10.1371/journal.pone.0012507.CrossRefGoogle Scholar
Nelson, R. J. (2005). An Introduction to Behavioral Endocrinology, 3rd Edn. Sunderland, Massachusetts, USA.Google Scholar
Nerrientet, E., Amouretti, X., MuÈller-Trutwin, M. C., Poaty-Mavoungou, V., Bedjebaga, I., Nguyen, H. T., Dubreuil, G., Corbet, S., Wickings, E. J., Barre-Sinoussi, F., Georges, A. J. and Georges-Courbot, M. C. (1998). Phylogenetic analysis of SIV and STLV type I in mandrills (Mandrillus sphinx): indications that intracolony transmissions are predominantly the result of male-to-male aggressive contacts. AIDS Research and Human Retroviruses 14, 785–96. doi: 10.1089/aid.1998.14.785.CrossRefGoogle Scholar
Norris, K. and Evans, M. R. (2000). Ecological immunology: life history trade-offs and immune defense in birds. Behavioral Ecology 11, 1926. doi: 10.1093/beheco/11.1.19.CrossRefGoogle Scholar
Olsson, M., Wapstra, E., Madsen, T. and Silverin, B. (2000). Testosterone, ticks and travels: a test of the immunocompetence-handicap hypothesis in free-ranging male sand lizards. Proceedings of the Royal Society of London, B 267, 23392343.CrossRefGoogle Scholar
Oppliger, A., Giorgi, M. S., Conelli, A., Nembrini, M. and John-Alder, H. B. (2004). Effect of testosterone on immunocompetence, parasite load, and metabolism in the common wall lizard (Podarcis muralis). Canadian Journal of Zoology 82, 17131719. doi: 10.1139/Z04-152.CrossRefGoogle Scholar
Owen-Ashley, N. T., Hasselquist, D. and Wingfield, J. C. (2004). Androgens and the immunocompetence handicap hypothesis: unraveling direct and indirect pathways of immunosuppression in song sparrows. American Naturalist 164, 490505.CrossRefGoogle ScholarPubMed
Pascal, M. and Castanet, J. (1978). Méthode de détermination de l’âge chez le chat haret des îles Kerguelen. Terre Vie 4, 529555.Google Scholar
Pontier, D. and Natoli, E. (1996). Male reproductive success in the domestic cat (Felis catus L.): A case history. Behavioural Processes 37, 8588. doi: 10.1016/0376-6357(95)00070-4.CrossRefGoogle Scholar
Pontier, D., Fouchet, D., Bahi-Jaber, N., Poulet, H., Guiserix, M., Natoli, E. and Sauvage, F. (2009). When domestic cat (Felis silvestris catus) population structures interact with their viruses. Comptes Rendus Biologie 332, 321328. doi: 10.1016/j.crvi.2008.07.012.CrossRefGoogle ScholarPubMed
Pontier, D., Fromont, E., Courchamp, F., Artois, M. and Yoccoz, N. G. (1998). Retroviruses and sexual size dimorphism in domestic cats (Felis catus L.). Proceedings of the Royal Society of London, 265, 167173.CrossRefGoogle ScholarPubMed
Pontier, D., Rioux, N. and Heizmann, A. (1995). Evidence of selection on the orange allele in the domestic cat Felis-Catus – the role of social-structure. Oikos 73, 299308. doi: 10.2307/3545954.CrossRefGoogle Scholar
Poulet, H. (2007). Alternative early life vaccination programs for companion animals. Journal of Comparative Pathology 137, S67S71. doi: 10.1016/j.jcpa.2007.04.020.CrossRefGoogle ScholarPubMed
Poulin, R. (1996). Sexual inequalities in helminth infections: a cost of being a male? American Naturalist 147, 287295. doi: 10.1086/285851.CrossRefGoogle Scholar
Povey, R. C. and Johnson, R. H. (1970). Observations on the epidemiology and control of viral respiratory disease in cats. Journal of Small Animal Practice 11, 485494. doi: 10.1111/j.1748-5827.1970.tb05599.x.CrossRefGoogle ScholarPubMed
Radford, A. D., Coyne, K. P., Dawson, S., Porter, C. J. and Gaskell, R. M. (2007). Feline calicivirus. Veterinary Research 38, 319335. doi: 10.1051/vetres:2006056.CrossRefGoogle ScholarPubMed
R Development Core Team (2009). R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. ISBN 3-900051-07-0, URL http://www.R-project.org.Google Scholar
Roberts, C. W., Satoskar, A. and Alexander, J. (1996). Sex steroids, pregnancy-associated hormones and immunity to parasitic infection. Parasitology 12, 382388. doi: 10.1016/0169-4758(96)10060-0.Google ScholarPubMed
Roberts, C. W., Walker, W. and Alexander, J. (2001). Sex-associated hormones and immunity to protozoan parasites. Clinical Microbiology Reviews 14, 476488. doi: 10.1128/CMR.14.3.476-488.2001.CrossRefGoogle ScholarPubMed
Roberts, M. L., Buchanan, K. L. and Evans, M. R. (2004). Testing the immunocompetence handicap hypothesis: a review of the evidence. Animal Behavior 68, 227239. doi: 10.1016/j.anbehav.2004.05.001.CrossRefGoogle Scholar
Rosenblatt, J. S. and Aronjon, A. R. (1958). The decline of sexual behavior in male cats after castration with special reference to the role of prior sexual experience. Behaviour 12, 285338.Google Scholar
Salvador, A., Veiga, J., Martin, J., Lopez, P., Abelenda, M. and Puertac, M. (1996). The cost of producing a sexual signal: testosterone increases the susceptibility of male lizards to ectoparasitic infestation. Behavioral Ecology 7, 145150. doi: 10.1093/beheco/7.2.145.CrossRefGoogle Scholar
Say, L. and Pontier, D. (2004). Spacing pattern in a social group of stray cats: effects on male reproductive success. Animal Behaviour 68, 175180. doi: 10.1016/j.anbehav.2003.11.008.CrossRefGoogle Scholar
Say, L., Pontier, D. and Natoli, E. (1999). High variation in multiple paternity of domestic cats (Felis catus L.) in relation to environmental conditions. Proceedings of the Royal Society of London, B 266, 20712074. doi: 10.1098/rspb.1999.0889.CrossRefGoogle Scholar
Schmid-Hempel, P. (2003). Variation in immune defence as a question of evolutionary ecology. Proceedings of the Royal Society of London, B 270, 357366. doi: 10.1098/rspb.2002.2265.CrossRefGoogle ScholarPubMed
Sheldon, B. C. and Verhulst, S. (1996). Ecological immunology: costly parasite defences and trade-offs in evolutionary ecology. Trends in Ecology and Evolution 11, 317321. doi: 10.1016/0169-5347(96)10039-2.CrossRefGoogle ScholarPubMed
Smith, L. C., Raouf, S. A., Brown, M. B., Wingfield, J. C. and Brown, C. R. (2005). Testosterone and group size in cliff swallows: testing the “challenge hypothesis” in a colonial bird. Hormones and Behavior 47, 7682. doi: 10.1016/j.yhbeh.2004.08.012.CrossRefGoogle Scholar
Sparger, E. E. (1993). Current thoughts on feline immunodeficiency virus infection. Veterinary Clinics of North America – Small Animal Practice 23, 173191.CrossRefGoogle ScholarPubMed
Sullivan, D. A. and Wira, C. R. (1979). Sex hormone and glucocorticoid receptors in the bursa of Fabricius of immature chickens. The Journal of Immunology 122, 26172623.CrossRefGoogle Scholar
Tanriverdi, F., Silveira, L., MacColl, G. and Bouloux, P. (2003). The hypothalamic-pituitary-gonadal axis: immune function and autoimmunity. Journal of Endocrinology 176, 293304.CrossRefGoogle ScholarPubMed
Veiga, J. P., Salvador, A., Merino, S. and Puerta, M. (1998). Reproductive effort affects immune response and parasite infection in a lizard: a phenotypic manipulation using testosterone. Oikos 82, 313318.CrossRefGoogle Scholar
Wedekind, C. and Folstad, I. (1994). Adaptive or nonadaptive immunosuppression by sex-hormones. American Naturalist 143, 936938.CrossRefGoogle Scholar
Wingfield, J. C., Hegner, R. E., Dufty, A. M. and Ball, G. F. (1990). The challenge hypothesis – theoretical implications for patterns of testosterone secretion, mating systems, and breeding strategies. American Naturalist 136, 829846. doi: 10.1086/285134.CrossRefGoogle Scholar
Wingfield, J., Jacobs, J., Tramontin, A., Perfito, N., Meddle, S., Maney, D. and Soma, K. (2000). Toward an ecological basis of hormone-behavior interactions in reproduction of birds. In Reproduction in Context (ed Wallen, J. and Schneider, J.), pp. 85128. MIT Press, Cambridge, MA, USA.Google Scholar
Xemar, V. (1997). Gestion sanitaire des populations de chats domestiques sur la ville de Nancy. Thèse vétérinaire. University of Lyon-1, France.Google Scholar
Yamamoto, J. K., Hansen, H., Ho, E. W., Morishita, T. Y., Okuda, T., Sawa, T. R., Nakamura, R. M. and Pedersen, N. C. (1989). Epidemiologic and clinical aspects of feline immunodeficiency virus-infection in cats from the continental United States and Canada and possible mode of transmission. Journal of the American Veterinary Medical Association 194, 213220.Google ScholarPubMed
Yamane, A., Doi, T. and Ono, Y. (1996). Mating behaviors, courtship rank and mating success of male feral cat (Felis catus). Journal of Ethology 14, 3544. doi: 10.1007/BF02350090.CrossRefGoogle Scholar
Zhang, H., Zhao, J., Wang, P. and Qiao, Z. (2001). Effect of testosterone on Leishmania donovani infection of macrophages. Parasitology Research 87, 674676. doi: 10.1007/s004360000354.CrossRefGoogle ScholarPubMed
Zuk, M. and McKean, K. A. (1996). Sex differences in parasite infections: Patterns and processes. International Journal for Parasitology 26, 10091023. doi: 10.1016/S0020-7519(96)00086-0.CrossRefGoogle ScholarPubMed